Threat of an Invasive Parasitic Fly, the Deer Ked (Lipoptena Cervi ), to the Reindeer (Rangifer Tarandus Tarandus): Experimental Infection and Treatment

Ann. Zool. Fennici 47: 28–36 ISSN 0003-455X (print), ISSN 1797-2450 (online) Helsinki 10 March 2010 © Finnish Zoological and Botanical Publishing Board 2010

Threat of an invasive parasitic fly, the deer ked (Lipoptena cervi ), to the reindeer (Rangifer tarandus tarandus): experimental infection and treatment

Sanna-Mari Kynkäänniemi1, Raine Kortet1,2, Laura Härkönen1, Arja Kaitala1, Tommi Paakkonen2, Anne-Mari Mustonen2, Petteri Nieminen2,3, Sauli Härkönen4, Hannu Ylönen5 & Sauli Laaksonen6

1) Department of Biology, P.O. Box 3000, FI-90014 University of Oulu, Finland 2) Faculty of Biosciences, University of Joensuu, P.O. Box 111, FI-80101 Joensuu, Finland 3) Faculty of Medicine, Institute of Biomedicine, Department of Anatomy and Cell Biology, P.O. Box 5000, FI-90014 University of Oulu, Finland 4) Finnish Forest Research Institute, Joensuu Research Unit, P.O. Box 68, FI-80101 Joensuu, Finland 5) Department of Biological and Environmental Science, Konnevesi Research Station, P.O. Box 35, FI-40014 University of Jyväskylä, Finland 6) Finnish Food Safety Authority EVIRA, Fish and Wildlife Health Research Unit, P.O. Box 517, FI-90101 Oulu, Finland

Received 12 Nov. 2008, revised version received 27 Nov. 2009, accepted 2 Oct. 2009

Kynkäänniemi, S.-M., Kortet, R., Härkönen, L., Kaitala, A., Paakkonen, T., Mustonen, A.-M., Niemi- nen, P., Härkönen, S., Ylönen, H. & Laaksonen, S. 2010: Threat of an invasive parasitic fly, the deer ked (Lipoptena cervi ), to the reindeer (Rangifer tarandus tarandus): experimental infection and treatment. — Ann. Zool. Fennici 47: 28–36.

Range expansion of ectoparasites can cause parasites to attack new host species. In these cases it is important for the parasite to be able to adapt to the new environment and to reproduce on the host. For the host, it is crucial to hinder successfully the development of long-lasting parasitic relationship. The deer ked (Lipoptena cervi) is a novel ectoparasite for northern cervids. We investigated if the deer ked can use the reindeer (Rangifer tarandus) as a host and, if it can, whether antiparasitic treatment against this parasite would be available. Three groups of reindeer were monitored: two groups of 6 reindeer were infected with 300 flies per each individual; a control group comprised 6 animals. One of the infected groups was treated with subcutaneous ivermectin. At the end of the experiment the infestation rate of the infected animals was low. The reindeer in the non-treated group had both live and dead deer keds and also a single pupa while the ivermectin-treated reindeer had only dead deer keds. As some deer keds survived and reproduced, the deer ked can potentially use the reindeer as a host but antiparasitic treatment may be effective against this parasite.

Introduction that suitable hosts are available, as parasites cannot exist in isolation from their hosts (Wall Invasion or range expansion of parasites requires 2007). Free-living invasive species have different Ann. Zool. Fennici Vol. 47 • Deer ked — a treatable threat to reindeer? 29 life histories as compared with those of inva- The moose has been a beneficial host species for sive ectoparasites (Boulinier et al. 2001): these the deer ked allowing it to widen its distribution, include better dispersal ability because of their as cervids are known to migrate long distances broader ecological requirements and tolerance (Cederlund & Liberg 1995). As the deer ked has (e.g. Mack et al. 2000, Sax & Brown 2000). spread rapidly towards the northern latitudes in When encountering a new host, the parasite needs Finland, it can be considered a host-dependent to overcome the physiological and immunologi- invasive species (Hackman et al. 1983, Kaitala cal defences of the hosts to be able to attach and et al. 2009). At present, the northern distribution reproduce successfully (Moore 2002, Wall 2007). limit of this louse fly is in the southern part of the For blood-feeding ectoparasites, which infest Finnish reindeer herding area, at approximately large vertebrates, host density is the most crucial 65°N (Kaitala et al. 2009) but there have been factor for the invasion, if these parasites use their occasional discoveries in areas situated two hun- hosts for dispersal (Boulinier et al. 2001). For dred kilometres further north. Outside the cur- these kinds of species, conditions on the host are rent range of the deer ked, there are suitable cli- usually stable with plenty of available resources. matic conditions and environments, where pupal Therefore, their distribution is most likely con- development would be possible and suitable strained by life history stages outside the host hosts available (Härkönen et al. 2010). (Lehane 2005). Thus, the new developing host- In addition to the moose, the deer ked can parasite relationships are affected not only by the utilize, e.g., the roe deer (Capreolus capreo- host and its resistance against parasitism but also lus) and the red deer (Cervus elaphus) as hosts by external climatic and biotic factors the life (Ivanov 1974). Samples collected recently from stage is exposed to outside the host (Wall 2007). skins of Finnish wild forest reindeer (Rangifer The effects of parasite infections on the host tarandus fennicus) and their bedding sites on the depend on the intensity of infection, the vir- snow contained deer keds or a few pupae, and ulence of the parasite and the resistance of the same was also observed for semi-domesti- the host animal (Moore 2002). Parasites can cated reindeer (R. t. tarandus) in the southern cause direct damage to the host’s tissues, carry part of the reindeer herding area (Kaunisto et zoonotic diseases and indirectly affect the energy al. 2009). Previously, Kettle and Utsi (1955) budget of the host by reducing its fitness. In observed reindeer infested with deer keds in general, host-specialist ectoparasites do only Scotland. Moreover, Ivanov (1981) reported that minor damage to the host, while it is commonly deer keds could also infect cattle (Bos taurus), assumed that non-specialist ectoparasites can be sheep (Ovis aries) and horses (Equus caballus) more virulent, especially when they infect new that grazed the forests in Belarus. The numbers host species (Wall 2007). of keds on cattle varied between 166 ± 12 and Arthropod parasites are usually ectoparasites. 315 ± 9 in 1973–1979 and 5–10 keds/cow were The deer ked (Lipoptena cervi) is an ectopara- sufficient to cause restlessness to the hosts. sitic louse fly capable of infecting various- cer The deer ked and some other louse flies differ vids (Haarløv 1964, Kaunisto et al. 2009). It from most other ectoparasites because they shed was detected in south-eastern Finland in the their wings after they have found a host animal. 1960s, presumably originating from Russia and Both female and male deer keds attack animals since then it has been spreading towards larger passing by and live on the host feeding on its areas in Finland (Hackman 1977, Kaitala et al. blood (Hackman et al. 1983). Reproduction of 2009). According to Reunala et al. (1980) Linné the deer ked takes place in the fur of the host described the deer ked in Sweden in the 18th animal and females deposit one puparium at a century. This louse fly entered Norway from the time (Haarløv 1964). It has been suggested that south-east in 1983 (Ottesen 2007). the breeding of the deer ked could last for up to In Finland, the principal host of the deer ked 8–10 months (Kaitala et al. 2007, but see Popov is the moose (Alces alces), usually with 2000– 1965). Adult deer keds emerge in the areas, 10 000 parasites per host in areas, where the deer where they dropped as pupae in the preceding ked is abundant (T. Paakkonen unpubl. data). autumn and winter (Haarløv 1964). 30 Kynkäänniemi et al. • Ann. ZOOL. Fennici Vol. 47

Also humans are susceptible to numerous 2007-03532/Ym-23) between 29 May and 13 attacks of the deer ked during professional or Dec. 2007. The experimental animals were 18 recreational forest use (Kortet et al. 2010). The adult reindeer (11 females and 7 males; age bites can cause allergic dermatitis and second- 2.8 ± 0.6 years). On 29 May, the reindeer were ary infections to sensitized individuals (Ivanov assigned into three experimental groups with 1974, Rantanen et al. 1982, Reunala et al. 2008). an equal sex ratio and average age (Infection The deer ked has also been proposed to act as group, Infection & Medication group and Con- a vector for bacteria of the Bartonella genus trol group). Each reindeer was fitted with a collar (Dehio et al. 2004). Deer keds are likely to with individual colouring and a numbered ear have stressful effects on their hosts and affect tag for identification. the health of animals by causing scratching and At the start of the experiment, on 29 May, associated skin changes (Ivanov 1981). Skin and before the reindeer were infected with deer keds, hide damages of moose have been connected the animals were treated against other possible to chronic deer ked infection (Laaksonen et al. endo- and ectoparasites with subcutaneous (sc) 2008a). ivermectin (0.2 mg kg–1; Bimectin vet®, Vet Antiparasitic treatment with ivermectin is pharma AB, Lund, Sweden/Vetcare Oy, Vantaa, routinely used in reindeer management in Fin- Finland) and topical deltametrin (75 mg/reindeer; land (Laaksonen et al. 2008b). Ivermectin is pour-on lotion on dorsal skin; Coopersect spot on a synthetic derivative of avermectins without vet®, Schering Plough, Ballerup, Denmark). The antibacterial activity (Dourmishev et al. 2005). It ivermectin treatment was repeated on 13 June. affects endo- and ectoparasites by preventing the The males were castrated on 29 May to prevent conduction of nerve impulses in synapses gated rut behaviour in autumn as it can be disturbing by glutamate or γ-aminobutyric acid causing and result in injuries or stress to other reindeer. eventual paralysis. In vertebrates, these synapses Moreover, the handling of males in rut can be are not located in the peripheral nervous system difficult. The reindeer were fed ad libitum with (unlike in invertebrates) but only in the central a commercial diet [Poron-Herkku, Rehuraisio, nervous system. As ivermectin cannot cross the Espoo, Finland, energy content 11.7 MJ metabo- blood-brain barrier it is harmless to vertebrates. lizable energy kg dry matter–1] supplemented As the deer ked is a potential threat to rein- with lichen (Cladonia spp.), hay and dried birch deer health and husbandry, this study focused (Betula spp.) and willow (Salix spp.) leaves. on two crucial questions: (1) are deer keds able The animals of Infection and Infection & to attach on reindeer and use them as hosts for Medication groups were immobilized in a han- feeding and reproduction, and (2) could this dling crib without sedation for the experimental parasite be controlled by using the antiparasitic infections. Each reindeer in Infection and Infec- agent ivermectin? The latter would be logisti- tion & Medication groups was similarly infected cally possible as the semi-domesticated reindeer on six occasions between 16 Aug. and 27 Sep. are regularly subjected to annual treatment and with an equal number of deer keds (35, 35, 35, medication against other ecto- and endoparasites 45, 35, 115, n = 300/reindeer; Table 1). The keds (Laaksonen et al. 2008b). were applied on the anterior back of each animal. The control animals were immobilized similarly but did not receive parasites. During the subse- Material and methods quent infections, signs of previously implanted deer keds were examined. Because there were Experimental procedures no previous data to indicate how the reindeer would react to the deer ked infection, we used The study was carried out in the Zoological Gar- infection intensity approximately 20 times lower dens of the University of Oulu, Finland (65°N, than previously observed in wild Finnish moose 25°E) with permission of the Committee on (T. Paakkonen unpubl. data). The number of deer Animal Experiments of the University of Oulu keds was relatively low in order to mimic the sit- (licence decision STH378A; 16.5.2007/ESLH- uation in nature in the southern reindeer herding Ann. Zool. Fennici Vol. 47 • Deer ked — a treatable threat to reindeer? 31 area and to avoid unexpected stress reactions of Results the reindeer. Some keds (n = 1260) were reared at the University of Oulu from wild-collected Immediately after the experimental infections the pupae from various parts of Finland (60–65°N). deer keds disappeared into the reindeer pelts and The numbers of deer keds used for the infection dropped their wings (Fig. 1a). During subsequent on specific dates depended on their hatching infection dates, live deer keds that had consumed rate. Due to the low emergence rate, deer keds blood (flat, more lightly-coloured, distended (n = 2340) collected by hand in the communes abdomen) and females that contained developing of Rantsila (64°N) and Liperi (62°N) were also larvae (round, dark, distended abdomen) could allocated equally to both infection groups. The be observed in the reindeer hair. In both Infection genders of the keds were not determined. All and Infection & Medication groups the reindeer reindeer groups were kept at natural ambient scratched themselves leaving bare patches and temperature and photoperiod in their own enclo- chafes in the pelt. Also hair discoloration caused sures (570 m2) to prevent deer ked contamination probably by deer ked faeces could be observed, between the groups. especially in white individuals. On 6 Nov. 2007, Infection & Medication No deer keds were found on Control group group was treated with sc ivermectin (0.2 at the end of the experiment (Table 2). Infection mg kg–1). Infection and Control groups were group had 6 ± 3 live and 5 ± 1 dead flies per given equivolume 0.85% saline injections as a reindeer (total 11 ± 3) and Infection & Medica- placebo treatment. The experiment was termi- tion group had no live but 17 ± 3 dead flies per nated between 10 and 13 Dec., and the reindeer reindeer. The total number of deer keds at the were stunned with a bolt pistol and killed by end of the experiment did not differ statistically exsanguination. An individual (ID no. 13) dis- between Infection and Infection & Medication playing strong stress, behavioural and physical groups (Mann-Whitney U-test, reindeer no. 13 reactions (i.e. hair loss) probably caused by the excluded: U = 10.0, n = 5–6, p = 0.429). The dif- infection, was killed earlier on 24 Oct. for ethi- ferences in the numbers of live (Mann-Whitney cal reasons. The pelts were examined in detail U-test, reindeer no. 13 excluded: U = 0.000, n by cutting the hair with scissors and calculating = 5–6, p = 0.004) and dead deer keds (Mann- the numbers of live and dead deer keds and other Whitney U-test, reindeer no. 13 excluded: U = possible ectoparasites. 3.0, n = 5–6, p = 0.030) between Infection group and Infection & Medication group were statistically significant. Those differences remained sig- Statistical analysis nificant also when reindeer no. 13 was included (data not shown). The differences in the numbers of live and dead The total recovery of deer keds in Infection deer keds between Infection group and Infec- and Infection & Medication groups was 4.7%: tion & Medication group were tested with the 1.1% for live and 3.6% for dead keds. The recov- non-parametric Mann-Whitney U-test using the ery of live deer keds in Infection group was 2.1% SPSS program (ver. 16.0, SPSS Inc., Chicago, (including reindeer no. 13). Only one pupa could IL). Differences were considered statistically be found from an individual reindeer of Infection significant at p < 0.05. The results are presented group. No other ectoparasites were observed in as mean ± SE. any of the study groups.

Table 1. Infection dates and numbers of transplanted deer keds/reindeer.

Group 16 Aug. 23 Aug. 4 Sep. 17 Sep. 20 Sep. 27 Sep. Total

Infection 35 35 35 45 35 115 300 Infection & Medication 35 35 35 45 35 115 300 Control 0 0 0 0 0 0 0 32 Kynkäänniemi et al. • Ann. ZOOL. Fennici Vol. 47

This conclusion is supported by field observations, where few pupae dropped on bedding sites of reindeer were observed in Hyrynsalmi municipality (65°N) in winter 2008 (Kaunisto et al. 2009). Our findings may have significant applications to reindeer herding, as deer keds have already expanded their northern distribution limit into the southern area of reindeer husbandry (Kaitala et al. 2009). Preliminary behavioural observations (S.-M. Kynkäänniemi unpubl. data) and data from another host species, the moose (Ivanov 1981, Laaksonen 2006), suggest that the deer ked could cause consider- able stress to its host. Due to strong indications of stress that may have been caused by the deer keds, one female reindeer in Infection group had to be killed for ethical reasons before the end of the experiment. From the point of view of invasive parasite species the situation can be described as follows: the deer ked, infesting primarily the moose in Finland, has reached areas where other cervids, such as the reindeer, are available as potential hosts. A dense moose population may be able to support the existence and spread of the deer ked in the north. However, for the alternative host species, the reindeer, this would mean an increasing number of deer ked attacks. Accord- ing to the present study, the deer ked, although Fig. 1. (a) A deer ked entering the fur on the dorsum of a reindeer during the experimental infection (photo: potentially irritating for reindeer, may not be Sauli Laaksonen). Note that the ked has not yet lost its well adapted to infest reindeer for longer peri- wings. The reindeer has denser winter pelage (guard ods. Thus, it is possible that slower adaptation of hair count 1700/cm2 on the back; Timisjärvi et al. 1984) the deer ked to the new host species or coevolu- 2 than the moose (250 hairs/cm ; Sokolov & Chernova tion with it could occur in the north where the 1987). (b) SEM image of a deer ked (photo: Paavo Niutanen). Note the shape and sharpness of the claws reindeer is at present the principal potential which enable attachment to the fur of the host. cervid host. An important factor regarding the possible health effects of the deer ked on the rein- Discussion deer is that the time period when host-seeking deer keds are the most abundant in nature is Our main results were: (i) deer keds seem to be during Aug.–Sep. (Ivanov 1981), immediately able to attach to reindeer and use them as hosts, after the mass appearance of other blood-con- and (ii) the parasitism could be controlled with suming insects (Helle & Tarvainen 1984). It ivermectin. However, the survival rates of the is known that summer disturbance caused by deer keds were very low and only a single pupa insects reduces the grazing time and increases was observed in the pelt of an individual rein- the energy expenditure of reindeer (Weladji et al. deer at the end of the study. Nevertheless, even 2003). Thus, a novel type of disturbance leading these low rates of survival and reproduction sug- to continuing insect harassment in autumn could gest that the deer ked could potentially become possibly affect reindeer winter survival in a dele- a parasite of reindeer and reproduce on them. terious manner. In the present study, bare patches Ann. Zool. Fennici Vol. 47 • Deer ked — a treatable threat to reindeer? 33 and chafes were observed in the fur, which could resistance against the sheep ked (Melophagus cause detrimental health effects especially in ovinus) in experimentally infected sheep (Nelson harsh winter conditions. For example, McLaugh- 1962). The density of hair in the winter pelage lin and Addison (1986) reported increased heat of the reindeer is higher than that of the moose loss and a poor physiological condition in cap- (Fig. 1a; Timisjärvi et al. 1984, Sokolov & tive moose with loss of winter hair caused by Chernova 1987). A very dense hair could hypo- attempts to remove winter ticks (Dermacentor thetically prevent the deer keds from gaining albipictus). sufficient access to skin for feeding on blood. It is worth noting that while deer keds were Reindeer might also be able to remove the deer recently observed in the Finnish reindeer hus- keds that are unable to intrude through the dense bandry area (Laaksonen et al. 2007, 2008a), the underfur even though the sharp claws of the deer dispersion of deer keds on reindeer further to the ked enable it to attach to hairs (Fig. 1b). This north could be limited by the seasonal feeding may also help another reindeer subspecies, the behaviour of reindeer herds. The reindeer graze wild-forest reindeer, to resist deer ked infec- in different areas in spring and autumn (Laakso- tion. An alternative cause for the decline in the nen 2006) and, thus, under this scenario, the flies numbers of live keds could be the complicated that have fallen in winter/spring as pupae would route of experimental transplantation (i.e. stored emerge in the next autumn in areas with less pupae and transported flies) causing an impaired seasonal reindeer grazing and could be unable to physiological condition of the deer keds used in find reindeer as hosts. However, the moose pop- the experiment. In addition, the natural course ulation is quite dense in the southern area of the of deer ked infection must also be taken into reindeer husbandry (Pusenius et al. 2008) and, account, as according to Ivanov (1981), the dura- thus, deer keds can possibly continue expanding tion of parasitism is between 120–180 days for their distribution area. an individual fly. Thus, it is possible that some of As the number of live deer keds on the rein- the flies used in the experiment had reached the deer decreased dramatically during the experi- end of their lifespan at the end of the study. We ment, it could be suggested that as compared did not observe any live deer keds from the pelts with e.g., the moose, the reindeer could have of Infection & Medication group, indicating that a natural ability to partly resist and discard ivermectin would be efficient against deer keds. deer keds from its skin similar to the partial It has a broad spectrum of antiparasitic activity

Table 2. The numbers of live and dead deer keds and pupae per study group (mean ± SE) and gender of the experimental reindeer at the end of the experiment on 10–13 Dec. 2007. a = this reindeer was removed from the experiment on 24 Nov. for ethical reasons. * = significant (p < 0.05) difference between Infection and Infection & Medication groups.

ID number and gender Live keds Dead keds Total Pupae

Infection 6 ± 3* 5 ± 1* 11 ± 3 1 04¥ 1 11 12 07¥ 2 6 8 12£ 10 1 11 1 13¥a 6 2 8 17£ 18 5 23 18¥ 1 3 4 Infection & Medication 0* 17 ± 3* 17 ± 3 0 01¥ 0 21 21 02¥ 0 27 27 05£ 0 10 10 10£ 0 26 26 11£ 0 10 10 15¥ 0 9 9 Control (3¥, 6£, 8¥, 9¥, 14£, 16¥) 0 0 0 0 34 Kynkäänniemi et al. • Ann. ZOOL. Fennici Vol. 47 against gastrointestinal nematodes, lungworms, as the reindeer, the development of a long-term warbles, mange mites and other nematodes and host–parasite interaction is a long-lasting adap- arthropods in cattle, other livestock and reindeer tive process. However, if the deer ked will be (Oksanen 1999). The endectocidid antiparasitic established in Lapland, it could cause an increas- treatment is at present routinely used in Finland ing threat of parasitism to the reindeer similar almost in the whole area of reindeer husbandry to southern Scandinavia, where the parasite can in late autumn and early winter, when the breed- be found in all available cervid host species (P. ing animals are treated with ivermectin. Thus, Välimäki unpubl. data). the impact of the deer ked on reindeer husbandry could probably be controlled but the high intensity of parasitism and potential disturbance on Acknowledgements wild cervids will possibly remain. So far, there is virtually no information available on the impact We want to thank Jari Ylönen, Milla Solismaa, Anu Ruo- homäki, Anna Honkanen, Pertti Rautio and the Biological of the deer ked on the health of wild cervids Research Facility Unit of the University of Oulu for their (but see Kaunisto et al. 2009). While ivermectin help during the experiment. For good comments on the man- seemed to be efficient against deer keds, more uscript we are grateful to Heikki Pöykkö and Sami Kivelä. studies on the basic biology of the species are We thank Paavo Niutanen for providing us the scanning required for the exact timing of the treatment. microscope images of the deer ked morphology. We thank also the University of Oulu, Vetcare Oy and the Ministry of Moreover, the effectiveness of the medication Agriculture and Forestry (Makera) for financial support. The against the deer ked in natural conditions and experiment complied with the current laws of Finland. against a higher number of parasites should be explored in controlled experiments without for- getting the possible emergence of drug resistance References against ivermectin (Shoop 1993) and environmental aspects (reviewed by Hrabok 2006). Beaumont, L. J. & Hughes, L. 2002: Potential changes in the The general pattern of the potential establish- distributions of latitudinally restricted Australian but- ment of the deer ked in northern environments terfly species in response to climate change. — Global Change Biology 8: 954–971. such as the Finnish Lapland may be that the Bequaert, J. 1953: The Hippoboscidae or louse-flies (Diptera) principal supporting or determining factors in of mammals and birds. Part I. Structure, physiology the spread of the deer ked are the climate change and natural history. — Entomologica Americana 32/33: together with the possible increase in moose 1–442. population densities. To support this, other ecto- Boulinier, T., McCoy, K. & Sorci, G. 2001: Dispersal and parasitism. — In: Clobert, J., Danchin, E., Dhondt, A. thermic species have been observed to widen A. & Nichols, J. D. (eds.), Dispersal: 169–179. 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